Correlates of healthcare-seeking behavior for acute gastroenteritis—United States, October 1, 2016 –September 30, 2017

Background In the United States, public health surveillance systems often underestimate the burden of acute gastroenteritis (AGE) because they only identify disease among those who interact with the healthcare system. Objective To identify factors associated with healthcare-seeking behavior among individuals experiencing community-acquired AGE. Methods From October 2016 –September 2017, we conducted a weekly, age-stratified, random sample of Kaiser Permanente Northwest members located in northwest Oregon and southwest Washington, United States. Individuals who completed the online survey and experienced AGE were included in the analysis. Univariate and multivariable logistic regressions were performed to identify predictors of healthcare-seeking behavior. Results Of the 3,894 survey respondents, 395 experienced an AGE episode and were eligible for analysis, of whom, 82 (21%) sought care for their AGE episode. In the final multivariable model, individuals with a concurrent fever (odds ratio [OR]: 4.76, 95% confidence interval [95% CI]: 2.48–9.13), increased diarrhea duration (≥6 days vs 1–4 days, OR: 4.22, 95% CI: 1.78–10.03), or increased vomiting duration (≥3 days vs 1 days, OR: 2.97, 95% CI: 1.22–7.26), were significantly more likely to seek healthcare. In the adjusted model, no sociodemographic or chronic disease variables were associated with healthcare-seeking behavior. Conclusion These findings suggest that individuals with a short duration of AGE and those without concurrent fever are underrepresented in healthcare facility-based surveillance systems.


Introduction
Most public health surveillance systems for acute gastroenteritis (AGE) are dependent on individuals with AGE seeking healthcare and, for assessing specific AGE pathogens, providing a stool specimen for diagnosis of their illness.However, most AGE episodes are mild and selflimiting, and as such, approximately 80% of individuals experiencing AGE do not seek care [1][2][3][4], and as few as 0.3% of individuals seek care and provide a stool specimen [5].While many studies have identified factors associated with healthcare-seeking behavior among children in developing countries [6][7][8][9][10], few have assessed factors associated with healthcare-seeking behavior in developed countries or across the full age spectrum [5,11].Understanding the factors that are associated with healthcare-seeking behavior can help surveillance systems more accurately estimate the burden of AGE and identify characteristics associated with underreporting.This information is essential to accurately interpret surveillance-derived data, which in turn helps guide public health prevention and resource allocation efforts.

Methods
To identify correlates associated with healthcare-seeking behavior we utilized data collected from the Community Acute Gastroenteritis (CAGE) Study conducted within an integrated healthcare delivery system of over 600,000 members in northwest Oregon and southwest Washington, United States [12].The study methodology has been previously described [13].In brief, from October 1, 2016 to September 30, 2017, 52 weekly, age-stratified, random samples of Kaiser Permanente Northwest (KPNW) members were recruited to complete an online survey pertaining to community acquired AGE.The survey collected sociodemographic information, the frequency of diarrhea and/or vomiting in the preceding 30 days, and the presence of any chronic gastroenteritis conditions.Among individuals reporting diarrhea and/or vomiting, information on symptoms, related healthcare-seeking behaviors, and treatments received were recorded.Separate surveys were used for minors (<18 years) and adults.For all minors <18 years a legal guardians provided informed consent and provided responses to the survey on their behalf.Information on insurance status and other pre-existing chronic diseases present at the time of survey completion were obtained from electronic health records.
Individuals were included in the analysis if they completed the online survey and reported an AGE episode, defined as three or more loose stools in any 24-hour period or any vomiting, in the last 30 days.Individuals with a self-reported chronic gastroenteritis condition who did not report any vomiting in the last 30 days were excluded from all analyses.A chronic gastroenteritis condition was defined as an illness lasting longer than 1 month in which diarrhea or vomiting is a major symptom, including irritable bowel syndrome, ulcerative colitis, and Crohn's disease.Healthcare-seeking behavior was defined as any reported contact with a health professional related to their AGE episode, including the following: call to nurse phone line, email to healthcare provider, video consultation with healthcare provider, in-person clinic visit, urgent care visit, emergency room visit, and admission to the hospital.
Differences in sociodemographic, clinical, and chronic disease factors among individuals who sought care and individuals who did not seek care were compared through chi-square tests.Age at the time of survey completion was categorized (<5, 5-17, 18-44, 45-64, �65 years).Prior to analysis, duration of diarrhea, maximum episodes of diarrhea in 24 hours, duration of vomiting, and maximum episodes of vomiting in 24 hours were recoded categorically to align with the modified Vesikari scoring system [14].In addition, race, insurance status, and age variables were collapsed to allow for adequate sample size for comparisons among groups.All other variables are presented as recorded in the survey.All variables with >10% of data missing were excluded from both bivariate and multivariable logistic regressions.
The final multivariable model was built using a forward selection approach.Independent variables were added to the model individually based on their ability to significantly improve model fit using Akaike Information Criterion values.All variables with a p-value <0.2 in univariate analyses were eligible for inclusion.Age and gender were identified as potential confounding variables a priori and were included in the model.Crude odds ratios (OR), multivariate adjusted odds ratios (aOR), and 95% confidence intervals (95% CI) were calculated using SAS v9.4 (SAS Institute; Cary, NC).
This project was reviewed and approved by the KPNW Institutional Review Board (FWA00002344).Participants provided informed consent to participate in this study.

Results
In total, 3,894 individuals participated in the CAGE study.After excluding respondents who did not experience AGE in the last 30 days (n = 3,422) and those with a chronic gastrointestinal condition who did not report any vomiting in the last 30 days (n = 77), 395 were eligible for inclusion in the analysis.
Of the 395 respondents with recent AGE, 82 (21%) sought care for their AGE episode.Among individuals who sought care, an in-person clinic visit (70%), calling the nurse phone line (56%) or visiting an urgent care clinic (34%) were the most common (Fig 1).Most respondents with an AGE episode that sought care had at least two different encounter types within the healthcare system, with 34%, 33%, 21%, and 13% reporting one, two, three, or four or more different healthcare encounter types, respectively, for their AGE episode.Most individuals (45%) had remote (email, video call, phone call) and in-person (visit with a doctor or clinic, emergency room visit, admission to hospital) care, while 21% received only remote care, and 34% only received in-person care.Individuals reported seeking care because their symptoms were bad (90%), their symptoms lasted a long time (79%), they wanted to know what made them ill (76%), or their home remedies did not make them feel better (64%; Table 1).
In the final multivariable model, diarrhea duration, vomiting duration, and fever were the only significant predictors of healthcare-seeking behavior among individuals experiencing AGE, with no sociodemographic or chronic disease variables significantly associated (Table 3).As diarrhea duration increased (�6 days vs 1-4 days, aOR: 4.22, 95% CI: 1.78-10.03)or vomiting duration increased (�3 days vs 1 day, aOR: 2.97, 95% CI: 1.22-7.26)individuals were more likely to seek care, while those not experiencing vomiting (0 days vs 1 day, aOR: 0.46, 95% CI: 0.21-0.99)were less likely to seek care.Individuals who had a concurrent fever with their diarrhea and/or vomiting were also more likely (OR: 4.76, 95% CI: 2.48-9.13) to seek healthcare.

Discussion
Similar to other work in developed countries (range: 19-36.5%), in this study, one out of every five individuals experiencing AGE sought care, with most having an in-person visit with a healthcare provider [1][2][3]5].Individuals were more likely to seek care as the duration of their diarrhea or vomiting increased, and if a fever accompanied their AGE symptoms.These findings align with individual's self-reported reasons for seeking care, which included that their symptoms were bad, lasted a long time, or that their home remedies did not make them feel better.In this study, no sociodemographic characteristics were significantly associated with healthcare-seeking behavior in our final multivariable model.
These findings support other work that has found that a long duration of illness [5,11], concurrent fever [2,5,15], longer diarrhea duration [2], and vomiting [2,16] were significantly associated with care seeking behavior in multivariable analyses.Other work has additionally shown other concurrent symptoms, including headaches [11] and abdominal cramps [15] to be associated with healthcare-seeking behavior, but these variables were not assessed in our study.While other studies have found that individuals with lower household incomes were more likely to seek care [2], 57% of our sample omitted responses to this variable and as such, household income could not be assessed as a potential healthcare-seeking factor in this *Values in columns may not sum to the total because of missing values. 1 Restricted to individuals �18 years old. 2 Restricted to women.study.While not significant in the bivariate or multivariable models, there was a higher proportion of males who sought care when compared to females, similar to previous work exploring healthcare seeking behavior for AGE [2,5].
In prior work, age is often associated with healthcare-seeking behavior with children (<5 years or <15 years) and older adults (65+ years) more likely to seek care when compared to other age groups [2,3,11,15,17].While age was not found to be a significant predictor in our final multivariable model, similar patterns were observed.Of note, when restricting the analysis to individuals experiencing diarrhea (with or without vomiting), children were significantly more likely to have healthcare-seeking behavior when compared to older adults (45-64 years).However, when limiting the analysis to individuals experiencing vomiting (with or without diarrhea) no association with age was observed in bivariate or multivariable models.Sample size prevented us from stratifying the analyses by age group.
In the healthcare setting, AGE treatment is often symptom-based, with little emphasis placed on finding the underlying cause of disease.However, 76% of individuals who sought care in this study indicated they did so in part to identify what made them ill.This desire on behalf of the patient may encourage the use of multi-pathogen detection assays, which could improve the patient's healthcare experience, reduce the inappropriate prescription of antibiotics, and enhance AGE surveillance efforts.
This work provides evidence that AGE surveillance systems are more likely to detect cases that have a longer duration of diarrhea or vomiting, or additional concurrent symptoms (e.g.fever).However, while these individuals may be more likely to interact with the healthcare system, as only 11 individuals who interacted with the healthcare system were asked to provide a stool sample (9 of which provided a sample), we could not assess if these factors were also associated with diagnostic testing (i.e.submitting a stool sample).The strengths of this study are that it was a random, age-stratified, sample of KPNW members.Similar to all studies of this nature, the results are subject to recall bias.With regards to limitations, it is possible that additional characteristics are associated with healthcare-seeking behavior but did not have sufficient sample sizes to be detected in this study and the limited sample size prevented stratification in the multivariate model.Additionally, information on several key predictor variables (e.g.income) were not reported by enough participants and were omitted from bivariate and multivariate models.Finally, this population was composed of KPNW members living in the United States, who are nearly all insured, as such these findings may not apply to uninsured populations or populations in other countries.

Conclusion
AGE surveillance systems based on interactions with the healthcare system likely underestimate the true burden of AGE in the population as only one in five individuals seek care for their AGE episode.AGE cases that seek healthcare are more likely to have had a longer duration of diarrhea, a longer duration of vomiting, and the presence of other concurrent symptoms (i.e., fever) when compared to individuals who are not detected.These findings can help guide further refinement and appropriate interpretation of AGE surveillance data, which in turn can be used to develop targeted interventions to prevent AGE.